We used dietary manipulations as well as manipulation of potential mate availability to investigate how male sexual signalling changes with current budget and previous expenditure. We found some cool results about what causes variation in age-dependent sexual signalling – these have implications for ‘honesty’ in sexual displays, and are also a nice reminder that there are simpler explanations than we (as humans, who love seeing patterns in the noise) often cling to.
Our paper also includes a nice example of using ‘zero-altered’ statistical models, enabling us to partition out effects on why males call from the effects on how long they call.
You can find the paper here, or email me for a PDF if you don’t have access to the journal.
Alternatively, the press office at Exeter put together a nice press release, which I’ve pasted below:
Shedding a few pounds might be a good strategy in the human dating game, but for crickets the opposite is true.
Well-fed male crickets make more noise and mate with more females than their hungry counterparts, according to research by the universities of Exeter and Stirling.
It has long been believed that males who acquire ample food can adopt a “live fast, die young” strategy – burning energy by calling to attract females as soon as they are able, at the expense of longevity – while rivals with poorer resource budgets take a “slow and steady” approach, enabling them to save resources and take advantage of their savings later in the season.
But the researchers found that increased diet – rather than any strategic decision by the cricket – led the best-provisioned crickets to chirp for longer. This had no noticeable cost to their lifespan.
Meanwhile hungrier males not only signalled less – meaning fewer female visitors – but also died younger.
Senior author Dr Luc Bussière, of the University of Stirling, said the findings offered a “simpler alternative” to understanding the behaviour of crickets.
“While it was intriguing to think that males might foresee and plan for their future reproductive prospects by strategically staying quiet, what our experiment suggests is actually easier to understand: rather than relying on an ability to forecast the future, crickets appear instead to respond mainly to the resources they have in hand,” he said.
Male crickets signal to females using an energetically expensive call, produced by rubbing together their hardened forewings.
The more time they spend calling, the more mates they attract.
The paper, published inFunctional Ecology, studied decorated crickets, which mate about once a day on average during their month-long adult life.
Males need a three-hour recovery period following each mating to build a new sperm package, after which they are able to call again in the hopes of attracting another female.
Researchers found that a male cricket’s decision about whether to call was primarily based on whether females were nearby – rather than how well-fed they were – but the better-nourished males were able to call for longer and thus increase their mating prospects.
The study also provides insights into how energy budgets keep male displays honest for choosy females over the course of the mating season.
“In nature, a ‘better quality’ male will likely have better access to resources,” said lead author Dr Tom Houslay, a Postdoctoral Research Associate at the University of Exeter.
“Low-quality males might be able to ‘cheat’ by calling a lot one day, making females think they are high-quality, but this is not sustainable – so there is ‘honesty on average’.
“A female may be fooled once or twice, but over time males with more energy will call more – meaning females should tend to make the ‘correct’ decision by preferring those males.”
That’s correct, friends – the two beetles you see in this image are both adult males of the same species of dung beetle, Onthophagus nigriventis. The chap on the right is clearly larger, and has a rather ostentatious horn extending from his thorax. This horn is a sexually-selected trait: horned males can use their armaments in battles over females, driving rivals away from mating sites, and even prying other males off a female whilst in flagrante. Sexual selection is all about the struggle to reproduce, and so traits are ‘sexually selected’ if their expression confers some benefit to the holder in terms of reproduction. In this case, large males with large horns are more likely to win battles with rivals, enabling them greater access to females, so there is a clear advantage to investing resources into weapons development.
Given that big, horned males fight rivals and guard their female partners (they may engage in the rather ungentlemanly pursuit of trapping lady beetles in mating burrows in order to have their way with them), then what the crap is going on with the guy on the left? Well, these horns are likely expensive in terms of resources, and any energy ploughed into growing horns is not available for investing in other traits – indeed, horns are known to trade off against morphological structures including eyes, antennae, and wings. Species of Onthophagus are well known for the size and diversity of their horns, but often these are only expressed by the largest ‘major’ males. What happens, then, if you’re a down-on-your-luck, resource-starved ‘minor’ male? Is there really any point in cashing in your precious metabolic chips for a gamble on a crappy little horn that’s never going to help you win any contests anyway? Surely there’s another strategy to be taken?
Indeed there is, and it’s called being a ‘sneaky fucker’*. While some males guard their mates, others will try to ‘sneak’ copulations with females. We now enter the realm of sperm competition: females may mate with multiple partners, so there is a battle amongst the sperm within her reproductive tract to fertilise eggs. If ejaculates are costly, males have to trade off resource investment on gaining fertilisation with investment on gaining additional matings. The more sperm ejaculated in a mating, the more eggs are likely to be fertilised – but, again, this requires resource investment. Furthermore, an increased risk of sperm competition should favour the evolution of increased expenditure on the ejaculate (i.e., the more likely that your little swimmers are going to be racing against some other dude’s, the more investment you should be making in ensuring your ejaculate is the biggest and best it can be).
In plain English (or, at least, an approximation thereof): if you’re a big horned dude protecting a little beetle harem, then you shouldn’t be all that worried about the fertilisation aspect – after all, you should be the only one for your ladies. You want to invest in lots of mating, not lots of ejaculate. Meanwhile, as a sneak, you’ve got to make those precious moments count, and ploughing your resources into the ejaculation makes sense – it’s in the female’s interests to have a few flings behind the dung-balls, so the greater the ejaculate, the better your chances of gaining fertilisations. Of course, the best way to produce larger amounts of ejaculate is to invest more resources into testis development.
All of which leads us nicely to what I think is one of the most ingenious (albeit slightly harrowing, once you really think about it) experiments I’ve read about while studying up for my PhD. Leigh Simmons and Doug Emlen (yes, this is another Doug Emlen-related post) cauterised those cells on beetle larvae which produce the thoracic horns in O. nigriventis, manipulating investment by ensuring that they could not grow these weapons. When compared to a control group comprising beetles allowed to develop normally, the cauterised individuals not only grew larger in size, but also developed disproportionately large testes. These results revealed the metabolic trade-off between horn development and both body size and testis size, in line with predictions from evolutionary models of ejaculate expenditure.
But what does this mean for the two beetles at the top of the page? Well, there’s a general tip here: if you’re going to sneak around, you’d better have gigantic balls.
*I’ve been told that Geoff Parker coined this phrase, but have been unable to find a reference for this, and during googling I accidentally clicked on ‘images’ and.. yeah. I need to keep safe-search on in future.
This post is a slightly modified version of an earlier entry on my ‘Nature!Sex!TopTips!‘ website.
Research blogging reference:
Simmons, L., & Emlen, D. (2006). From the Cover: Evolutionary trade-off between weapons and testes Proceedings of the National Academy of Sciences, 103 (44), 16346-16351 DOI: 10.1073/pnas.0603474103
Blatant plug: I am really interested in the intersection between sexual selection and life-history allocation – the way that individuals invest their resources – and (along with my long-suffering supervisor) have written an article on this topic for Wiley-Blackwell’s Encyclopedia of Life Sciences online journal. You can find it at the following link, or drop me a line if you would like a copy:
I’m going to skip ahead in my review of the talks which I enjoyed at Evolution 2012 in Ottawa, as Doug Emlen‘s latest research has just been published in the latest issue of the prestigious journal Science. This gives me an excuse to write about his talk and the new paper, as well as to engage in gratuitous posting of beetle photos.
I have a real soft spot for research on beetle horns, as followers of Nature!Sex!TopTips! may be aware, so I was really excited to see Emlen’s talk – even more so after the taster that was Erin McCullough’s presentation earlier in the week (McCullough is a PhD student co-supervised by Emlen and Bret Tobalske at the University of Montana’s ‘Flight Lab’). Research into animal weaponry often goes hand-in-hand with studies of ornaments because there is direct sexual selection upon them; females use ornaments as a basis on which to select a mate, while weapons are used by males to defeat rivals (or to assess their condition and status) and so gain access to females. Together, these exaggerated, elaborate structures are some of the most incredible sights we see in nature.
It’s no surprise that a lot of research investigates these amazing traits, but there are still some big questions to grapple with. For example, they seem to be very reliable indicators of male quality – why should this be so? Can’t some males ‘cheat’ by somehow investing more into ornament or weapon growth than other things? Also, if females select upon a particular heritable trait, then shouldn’t we see very little variation by now, with all males having pretty much the same size of trait? Consider the range of deer antler size in comparison to, say, the range of deer leg length. Antlers are much, much more variable – but why?
I’ve written about the maintenance of genetic variation in such traits before, both here and over at the Nothing in Biology Makes Sense blog, using the ‘genic capture’ model proposed by Rowe and Houle. This model posits that the continued evolution of sexually selected ornaments and weapons is enabled by these traits ‘capturing’ the underlying condition of the animals. An individual’s condition is affected by its general health, nutrition, parasite resistance, competitive ability, etc… essentially, the genetic variation among males in terms of all these factors underlies the variation in these amazing traits. It’s this ‘condition-dependence’ of traits, a close association with the individual’s condition, which means that the expression level should be ‘unfakeable’ and thus a reliable indicator of male quality. Not only this, but it also allows the evolution of ever-more exaggerated ornaments and armaments. So, these traits have some particular characteristics which have triggered huge interest from an evolutionary point of view: extreme size, heightened sensitivity to condition, and much more variability than we see in other morphological traits. We often think of condition-dependence as a kind of ‘black box’ – environmental and genetic factors go in, and traits come out. Emlen’s current research asks the question of, well, what mechanism enables this to happen? What’s inside the black box that creates these incredible, extreme biological structures?
Emlen proposes that there is a developmental explanation for this, and it lies within the insulin / insulin-like growth factor (IGF) pathway. This pathway has emerged as the central mechanism in animals for integrating physiological condition with growth; insulin and IGFs not only regulate tissue growth and body size, but they are also sensitive to factors such as nutrition, stress and infection. The levels of insulin / IGF circulating in an individual would cause a graded response via this particular pathway, with growth speeding up or slowing down in response to changes in nutritional or physiological state – i.e., the same kind of factors which affect what we term ‘condition’. So far, so straightforward, you might think: there’s a pathway which controls tissue growth that depends on how healthy and well-nourished you are. But how might this lead to the evolution of highly exaggerated weapons and ornaments?
Well, here comes the even cooler bit: traits differ in how they respond to these signals. This can have a truly profound effect on the amount and nature of their growth. Some traits, like Drosophila genitalia size, are not particularly sensitive to insulin / IGF signalling, meaning that they tend to be around the same size in all individuals, no matter their nutritional state. Wings, meanwhile, are more sensitive to these signals. Within a variable population of fruit flies, with a normal range of body sizes, we would see variation in wing size approximately equal to variation in body size, while genitalia size would hardly vary at all. So, just as wings are more sensitive to insulin signalling in Drosophila than are genitals, Emlen predicted that exaggerated weapons or ornaments are even more sensitive than that. Such heightened sensitivity to insulin / IGF levels would explain how such traits grow to extreme sizes, why there is such huge variation within populations, and why such traits seem to be reliable indicators of underlying quality.
Emlen and his colleagues tested this hypothesis in male rhinoceros beetles (Trypoxylus dichotomus), which have a large forked horn on the top of their head. They used RNA interference (RNAi) to perturb transcription of the insulin receptor (InR) – that is, they simply stopped this particular signalling pathway from working properly. They did this at the beginning of metamorphosis, a point when body size is no longer growing, but adult structures – such as genitalia, wings, and the huge sexually-selected horn – are. If increased cellular sensitivity to insulin / IGF signalling is at least partly responsible for the evolution of this exaggerated horn in these beetles, then horns should be more sensitive than wings to the experimental manipulation of the pathway activity via RNAi. Furthermore, Emlen and his team predicted that – just as with fruit flies – genitalia should be relatively insensitive to this disruption of insulin / IGF signalling.
Results showed that the genitalia of males whose InR pathway activity was disrupted did not show a significant reduction in size when compared to control males (which did not undergo the RNA interference treatment). Meanwhile, the wings of RNAi treatment males showed a significant reduction in size that measured around 2% in comparison to control males. This is typical of the majority of ‘metric’ traits, such as eyes, legs, etc. Horns, however, predicted to be the most sensitive to nutritional state, suffered a significant reduction of around 16% in RNAi treated males relative to control animals. This eight-fold increase in sensitivity of horns in comparison to wings is highly consistent with Emlen’s model of the evolution of exaggerated trait size from heightened sensitivity to this particular pathway – giving us a real insight into the black box of condition-dependence, and how such incredible traits evolved.
Note: I highly recommend reading the paper itself, not only because it’s very well-written, but also because Emlen does a great job of summarising models of sexual selection and condition-dependent traits, and the impact of this latest research on those models. Plus there’s some nice beetle pictures in there, and you love nice beetle pictures. DON’T YOU?
This month saw the long-awaited publication in PLoS ONE of a paper describing the courtship of the peacock spider Maratus volans, a tiny arthropod whose displays have helped it achieve the heady heights of internet fame over the past couple of years (well, at least in those parts of the internet where people like to watch videos of little animals dancing around). Girard and her fellow researchers used high-speed video recordings and laser vibrometry to show that male spiders use vibratory signals in addition to ornamentation and motion displays in order to attract a mate.
I have written previously on how males and females invest different amounts of resources in their gametes (sperm and eggs), and how this imbalance creates the conditions for sexual selection – Darwin’s proposed mechanism for the evolution of different body shapes and sizes across the sexes. Sexual selection covers both female choice and male competition, scenarios that have led to the development of exaggerated male ornaments and weaponry respectively (consider, for example, the beautiful train of the peacock, or the fierce antlers of stags).
While weaponry is used to fight or simply intimidate opponents (as well as the rather ungentlemanly acts of prising rival males from females mid-copulation, and trapping females in mating burrows, as is the wont of some beetles), ornaments serve to impress and seduce the watching female. Highly-ornamented species are often those in which both sexes mate with multiple partners, with males offering nothing more than their sperm – not for them the worries of caring for offspring, or providing food and territory for their mate*. The displays that males engage in often serve to highlight their ornaments – male greater sage grouse Centrocercus urophasianus are a prime example:
This type of behaviour is especially evident in ‘lekking’ species, where males gather on a display ground (the lek) and parade their wares to potential partners. Only those males with the very best ornaments are deemed good enough by the choosy females, and each will likely mate with multiple partners – meaning that the genes of a select few sires are making it into the next generation. This leads us to the essence of the ‘lek paradox’: if females are selecting males on the basis of certain trait values, this should erode genetic variation in these traits, meaning that all traits should converge to similar values. If all traits were the same, females would be unable to choose between males, and – more importantly – there would be no point in trying to do so. I like to remember this paradox through the reappropriation of the lyrics to a popular song:
However, there is plenty of evidence to show that female choice on the basis of sexual traits persists. So, how can we explain the maintenance of genetic variation for sexual traits? One proposed mechanism is that ornaments develop a strong relationship with an individual’s ability to acquire resources from its environment and convert them internally to usable forms – a relationship known as ‘condition-dependence’. This ability includes factors such as fighting disease, catching prey, foraging, and metabolising nutrients. All the genes underlying these factors are associated with the sexual trait due to condition-dependence, and so the trait serves as an indicator of how the vast majority of an individual’s genome is performing in its current environment. Rather than eroding the variation in a few genes that encode a trait, selection is now based on the vast variation of virtually the entire genome. Not only that, but changes in the environment will alter which genotypes perform best, and mutations in any area of the genome will have some effect on mating success.
While the paradox is named after lekking species, which often provide the most extreme examples of ornamentation, the problem extends to all those species where males do not give their partners direct (or ‘material’) benefits. Research in this field helps us to figure out the wider effects of sexual selection – for example, can it help to prevent the build-up of deleterious mutations in a population? On a different level, it is interesting to ask why such behaviour exists – is sex really worth the male making himself quite so obvious to predators? How does a female ‘know’ which male is ‘good enough’? This paper gives us a nice description of the courtship behaviour that we see in this video, and provides a basis for further study of these charismatic little animals (and others in the genus Maratus) – this is especially intriguing as the ‘multi-modal’ nature of their courtship is ripe for further investigation. Each facet is a drain on resources, whether it be the development of the colourful abdominal flaps and ornamented third legs, or the waving and dancing itself – to say nothing of the vibrational drumming, wonderfully described as ‘rumble-rumps’ by the paper’s authors. Why have the males evolved these multiple signals? Do they represent different features of his quality, and can females discriminate between them? Is one signal more important than all the rest? I’m sure I’m not the only one who’s excited about what else this colourful spider can inform us about evolution.
See more videos from the Elias lab at Berkeley here.
Check out Jurgen Otto’s fantastic photographs here.
*Note: I could not find much detail in terms of the mating system in Salticidae, much less this particular species, so it may indeed be that males are providing females with direct benefits. In which case, ignore me.
Think of a duck. Chances are, you’re picturing a mallard – and, if you weren’t, you probably are now. Imagine the male with his striking green-blue head, and the comparatively drab, mottled brown female. If you are a regular reader of science blogs, or simply a fan of waterbird genitalia, your mind may wander to his 20cm-long explosive corkscrew penis, or her cavernous vagina, riddled with dead ends and hairpin bends.
The father of modern taxonomy himself, Carl Linnaeus – admittedly, without having gained privy to these reproductive organs – first classified the male and female mallards mistakenly as separate species. We accept these differences readily nowadays, but how and why have they occurred? Even stranger, why should any species evolve such elaborate reproductive organs?
The answer stems from ‘gametes’, or reproductive cells. Males are defined by carrying sperm, millions of pared-down parcels transporting genetic cargo at high speed. Meanwhile, females harbour relatively few eggs, sluggish monoliths packed with nutrients and protection, waiting patiently for one battling sperm to fuse the genetic information and produce a new organism.
This imbalance in the resources ploughed into gametes results in conflicting desires in the sexes. A male could incur little cost by mating with as many females as possible, increasing the probability of his genes passing to the next generation. His female counterpart, having invested so much in her eggs, gains more from exercising restraint to ensure her offspring are of the highest possible genetic quality.
By what means, then, can a female determine her perfect match? Darwin outlined such characteristics in his 1871 book ‘Selection in Relation to Sex’:
“…the greater size, strength, and pugnacity of the male, his weapons of offence or means of defence against rivals, his gaudy colouring and various ornaments, his power of song, and other such characters.”
This system can be as straightforward as the bull elephant seal using his great strength to drive rivals from a harem of females. Other traits proved far more puzzling – Darwin’s frustration in the years prior to this publication is summarised in an 1860 letter containing the epithet:
“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”
One theory is that such traits indicate genetic quality by acting like handicaps. Bright colours, displays and songs attract predators, while a cumbersome tail hinders a quick getaway. A male may be indicating, “Hey, if I have such a big handicap and I’m still here, doesn’t that show you how great I am? You should probably have my babies.”
What happens, then, to those that cannot compete at the highest level – should they simply give up? No, instead they engage in some downright sneaky behaviour, such as yellow dung flies waiting at the edge of a dung heap, ready to pounce on unsuspecting females travelling to meet Mr. Right atop a delicious pile of excrement. On the Hawaiian island of Kauai, Professor Marlene Zuk discovered that the mate attraction ‘song’ of the field cricket – produced by males rubbing their wings together – had enabled an invading parasitic fly to target the species ruthlessly. Rather than face extinction, however, this cricket population rapidly evolved to favour a mutation that removed rough edges from the wings. These smooth, silent crickets possess no real powers of attraction, instead surrounding the remaining chirpers in the hope of engaging a prowling female. While she would prefer a personal serenade from her potential mate, waiting too long exposes her to greater danger – or the risk of being ‘left on the shelf’. There is such a thing as being too choosy, after all.
Another tactic is to offer a ‘nuptial gift’, which can be an edible treat that the male produces himself. This has led to the synthesis of offerings that lower the female’s desire to remate before his sperm have completed fertilisation. ‘Aggressive sperm’ may outcompete or kill off rival gametes, while a dragonfly penis can scoop out existing seminal fluid. The bumblebee, meanwhile, breaks off its penis in the queen to form a ‘vaginal plug’ – an extreme case of putting all your eggs in one basket, if that’s not too confusing an analogy given the topic at hand.
It would be foolish to presume, however, that females have been standing by idly in evolutionary terms. Insects such as water striders and seaweed flies are locked in a race whereby females evolve anti-grasping functions just as the males develop claspers. Indeed, the mallard’s complex vagina has evolved as a defence mechanism. As the female is victim to frequent attempts at forced copulation, this not only helps to prevent entry, but also diverts unwanted sperm away from those precious eggs.
This arms race has raged ever since sex first evolved. As long as males and females continue searching for the tiniest advantage over one another, the battle of the sexes shows no sign of slowing down.
Recently, probably due to the incredible macro photography of Igor Siwanowicz that I linked to recently, I’ve become rather obsessed with mantises. Before then, I’d paid very little attention to these weird creatures, and will admit to having been mildly terrified of them in the past. This stemmed from an unfortunate incident many years ago, when I tried to brush one off the door handle of a holiday apartment, only to learn that they can fly – and can propel themselves rapidly towards a human face. The neighbours came rushing out because they had heard what they assumed to be the cleaning lady screaming. Anyway, possibly due to this, I thought that there was just a ‘praying mantis’, and had no idea that the order could range from this:
…and many more incredible shapes, sizes and colours. The displays that a mantis can produce when threatened are really quite incredible, and I have been told that they are great for use in undergraduate practical classes. Mantises are apparently relatively short-sighted, and so two can be placed on opposing ends of a mounted piece of string, and it will suddenly become very clear when they notice each other. Unfortunately, the ‘loser’ will signify defeat by flying off to a remote corner of the classroom, delaying the end of the lesson as the tutor (or, more likely, a hapless TA) climbs up to gingerly retrieve it. Here are two videos of different mantis displays, the first relying on sound and wing movement, the other on the large peacock-style eyes on its wings:
So, what wonders does the mantis have in store for the intrepid sex researcher? Rather distressingly, the answer is sexual cannibalism. Males are smaller than females, which have voracious appetites and can eat up to 16 crickets per day, and so put themselves in a rather precarious position both prior to and during copulation. There is a lot of evidence, including the video below (complete with rather breathless commentary), of females devouring their mates during intercourse, but a controversy remains over the function of this.
Does the male, as in the case of the redback spider, allow himself to be eaten in order that the bearer of his children has a large meal when times are scarce, therefore helping to furnish his offspring with added nutrition? Some other insects allow females to ‘nibble’ on them during sex, thus lengthening the duration of copulation and enabling more sperm to enter the female and fertilise the eggs – could it be that this is a poorly-judged version of this adaptation? The latter seems unlikely, as females generally remove the head first, and although the body continues its final mindless act, studies have shown that ejaculation tends to happen more rapidly after decapitation, if at all.
A 2010 study by Kate Barry, of Macquarie University in Sydney, Australia, investigated the state of female nutritional status on mating dynamics in a sexually cannibalistic praying mantid. Previous studies have shown that scramble competition is important in these mating systems, and thus males are selected for their ability to detect and locate females. Given that each copulation holds the risk of death for the male (and the inherent fitness costs of this occurring), and that condition has been shown to be positively correlated with fecundity in female mantises, then theory would predict the evolution of strong male choice for females in good condition. A female in good condition is not only likely to have more eggs, making her a good choice for a male wanting to ensure that he makes the most of the copulation should it be his last, but is less likely to be starved of food. Interestingly, Barry found that long-distance male attraction to females is somehow linked to female fecundity, with ‘low condition’ females still being attractive to males as long as they had a base level of fecundity. Nutritional status seemed to have no bearing on male choice, and so it would appear that females may produce a pheromone that indicates fecundity. Indeed, in a species of cockroach there exists a relationship between ovarian development and pheromone production, meaning an honest signal is produced to demonstrate a female’s egg-bearing capacity.
It would seem, then, that the unfortunate decapitated males may be those that were unable to secure copulation with high-fecundity females, and sacrificed themselves in a final desperate attempt to pass on their genes. Or perhaps, as can happen in many species, they simply read the signals wrongly.
Note: since becoming more interested in the mantis, I’ve even come so far around as to having decided to place an order with Ornamental Insects for a ghost mantis, after listening to their interview on John F Taylor’s Reptile Living Room radio show. However, you may be able to tell from the picture below that, perhaps, I haven’t quite conquered my fear outright…